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Sains Malaysiana 43(12)(2014): 18731882

Decomposition Process and Post Mortem Changes: Review


(Proses Pereputan dan Perubahan Pasca Kematian: Ulasan)

TEO CHEE HAU, NOOR HAZFALINDA HAMZAH, HING HIANG LIAN & SRI PAWITA ALBAKRI AMIR HAMZAH*

ABSTRACT

Decomposition is degradation process of a corpse into basic respective constituents macroscopically and microscopically
by action of microorganisms, arthropods and scavengers. Post mortem changes could be separated into early post
mortem changes (i.e. algor mortis, rigor mortis and livor mortis) and putrefaction stages of corpse. These changes
function as suitable indicators for determination of post mortem interval (PMI). In this paper, different stages of post
mortem changes, possible variations such as mummification and formation of adipocere and special circumstances such
as burial condition is discussed. This article also refers to several arguments in the different texture of adipocere and
the influence of different types of fabric in affecting the post mortem changes and formation of adipocere. This is largely
due to the property of permeability and resistance of material against degradation process. Undeniably, decomposition
process involves numerous potential variables including burial condition, presence of clothing, potential formation of
adipocere and mummification. Hence, studies in forensic taphonomy combined with real case scenario are crucial in
understanding the nature of decomposition and estimation of PMI with higher accuracy.
Keywords: Adipocere; burial condition; decomposition; mummification; post mortem changes; putrefaction
ABSTRAK

Pereputan adalah proses penguraian mayat kepada bahan asas secara makroskopik dan mikroskopik melalui aktiviti
mikroorganisma, atropod dan pembangkai. Perubahan pasca kematian dapat dibahagikan kepada perubahan pasca
kematian awal (iaitu algor mortis, rigor mortis dan livor mortis) dan tahap pembusukan mayat. Perubahan ini berfungsi
sebagai petunjuk yang sesuai bagi penentuan selang masa pasca kematian. Dalam ulasan ini, tahap perubahan pasca
kematian yang berbeza, variasi seperti mumifikasi dan pembentukan adipocere serta situasi tertentu iaitu keadaan
pengebumian telah dibincangkan. Artikel ini juga merangkumi beberapa pendapat yang bertentangan terhadap perbezaan
antara tekstur adipocere yang terbentuk serta pengaruh faktor jenis pakaian yang berbeza dalam mempengaruhi
perubahan pasca kematian dan pembentukan adipocere. Ini adalah disebabkan oleh tahap ketelusan dan ketahanan
bahan terhadap proses pereputan. Tidak dapat dinafikan, proses pereputan melibatkan pelbagai faktor yang berpotensi,
termasuklah keadaan pengebumian, pakaian, pembentukan adipocere dan mumifikasi. Maka, kajian dalam forensik
tafonomi bersama dengan senario kes sebenar adalah penting untuk memahami proses pereputan dan penentuan selang
masa pasca kematian dengan kejituan yang lebih tinggi.
Kata kunci: Adipocere; keadaan pengebumian; mumifikasi; pembusukan; pereputan; perubahan pasca kematian
INTRODUCTION
Decomposition is a natural process that occurs for every
organism that has died. Initially, the degradation may not be
visible to the naked eye as the process starts at the cellular
level. Slowly the changes will progress to macroscopic
and form the post mortem changes. This process continues
even beyond the dry remains stage as the bones still
undergo decomposition although at a much slower rate
as previously seen. In the end, the whole decomposition
process allows the recycling of energy flow and nutrient
into the surrounding ecosystem (Fenoglio et al. 2010;
Tibbett & Carter 2009).

The understanding of post mortem changes is crucial
for estimation of post mortem interval (PMI). PMI is the
interval of time that has passed since the deceased passed
away until the corpse was found (Parsons 2009; Poloz &

Oday 2009). Generally, the longer the time of death has


occurred, the less accurate the PMI estimate would be.
Once the corpse has reached the dry remains stage, the
estimation of PMI could be difficult due to influence of
various environmental factors (Dautartas 2009; Kaliszan
et al. 2009). Estimation of PMI is very important in crime
investigations, event reconstructions and solving cases
because an accurate time of death can help the courtroom
in accepting or denying statements and alibi of suspects
and witnesses. There are many ways in determining PMI
for victims. Madea (2005) categorized the methods of PMI
estimation into quantitative or subjective in nature and
whether there is presence of independent variables or only
based on assumptions.

It is undeniable that breaking down of tissue bulk to
their building blocks takes time and the duration largely

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depends on intrinsic and extrinsic factors. Intrinsic factors


include age and physical size of corpse, ante mortem
medical condition and presence of trauma. Extrinsic
factors on the other hand, include variation in surrounding
temperature, weather, burial, clothing, presence of
arthropods and scavengers. The progress of decomposition
could be measured or quantified by a series of methods.
These include carcass mass loss, carbon dioxide-carbon
evolution, ninhydrin-reactive nitrogen, microbial biomass
carbon and faunal succession pattern, etc (Carter et al.
2008a; Spicka et al. 2011). These methods in evaluating
the progress of decomposition are crucial to indicate the
extent of tissue degradation hence in estimation of PMI.
AUTOLYSIS AND PUTREFACTION

Generally, the decomposition process occurs by two


mechanisms, which are autolysis and putrefaction (Dent
et al. 2004; Janaway et al. 2009a). Autolysis is a cellular
self-destruction process caused by hydrolytic enzymes
that were originally contained within cells (Enwere 2008;
Shirley et al. 2011). Autolysis normally begins at cells,
which are metabolically active or contain large amount of
water, lysosomes and hydrolytic enzymes. Organs that are
involved in high adenosine triphosphate (ATP) production
and membrane transportation such as liver and brain are
also more susceptible to autolysis reaction as compared to
other organs (Gennard 2007; Swann et al. 2010b). At this
level, the degradation can only be observed at histological
level (Enwere 2008; Janaway et al. 2009a).
Shortly after pulmonary and cardiovascular system
stops, supply of oxygen to cell ceases and continued
depletion of oxygen concentration will lead to anaerobic
condition within the corpse (Swann et al. 2010b; Zhou
& Byard 2011). In order to maintain basic cellular
metabolic activity, anaerobic mechanism glycolysis serves
as an alternative source of energy and produces waste
products such as carbon dioxide and lactate. The cellular
pH drops until the membrane is unable to maintain its
normal permeability and rupture accompanied by release
of hydrolytic enzymes (Paczkowski & Schtz 2011;
Parkinson et al. 2009). The free hydrolytic enzymes will
start to attack any cellular structures which under living
condition are not considered as substrate (Powers 2005).
Consequently, cellular membrane ruptures and cellular
junction breaks down, releasing cellular content (Parsons
2009; Zhou & Byard 2011). The released cellular content
functions as source of nutrient and energy for subsequent
microbiological reaction in putrefaction process (Parkinson
et al. 2009; Zhou & Byard 2011).
On the other hand, putrefaction is degradation of
tissue by microorganism activity, such as bacteria, fungi
and protozoa, which originate from normal biota in human
body especially in gastrointestinal tract (Dent et al. 2004;
Paczkowski & Schtz 2011). The process of putrefaction
could be accelerated if there are certain ante mortem
conditions on the deceased, especially sepsis (either
systemic or localized) which will increase the bacteria

load in the corpse even prior to invasion of environmental


microorganisms (Adams 2009a; Zhou & Byard 2011). On
the other hand, the relative sterility of newborn allow them
to deviate from the normal putrefactive process and hence
no bloating could be observed in some cases (Mcquinn
2011; Schotsmans et al. 2011b).

Most post mortem changes by putrefaction are visible
macroscopically such as discoloration of skin and bloating
of body parts. The decompositional product formed by
putrefaction may appear in gas, fluid or salt form. Examples
of gaseous product include hydrogen sulfide, carbon
dioxide, methane, ammonia, sulfur dioxide and hydrogen
(Gennard 2007; Vass 2001). Other forms of product include
skatole, indole, methylindole, cadaverine, putrescine,
various hydrocarbons, nitrogen containing, sulfur
containing and phenolic compounds (Dekeirsschieter
et al. 2009; Vass et al. 2008). Accumulation of these
decompositional (particularly gaseous) products will then
lead to swelling at anatomically spacious body parts such
as face and abdomen.
EARLY POST MORTEM CHANGES

Post mortem changes occur in early and late phase. Early


post mortem changes include algor mortis, rigor mortis
and livor mortis while late post mortem changes involve
breakdown of soft tissue leading to noticeable macroscopic
changes (Lee 2009; Swift 2006). For corpse that remain in
fresh stage, PMI is mostly estimated through examination of
algor mortis, livor mortis and rigor mortis (Poloz & Oday
2009; Tibbett & Carter 2009).
Algor mortis is the process of decreasing of body
temperature to ambient temperature (Parsons 2009; Reddy
& Lowenstein 2011). A corpse loses heat through four
mechanisms, which are radiation, convection, conduction
and evaporation of any fluid on corpse (Myburgh 2010;
Shkrum & Ramsay 2007). The rate of cooling could be
plotted against time after death as a sigmoid curve. Initially,
there is a lag phase where body temperature remains stable
for a period before the rate of cooling becomes linear and
slowly decreases until it reaches equilibrium with ambient
temperature (Myburgh 2010; Swift 2006).

Generally, larger difference between body temperature
and surrounding temperature will lead to more rapid
cooling of temperature (Adams 2009b; Shkrum & Ramsay
2007). However, the decrease of body temperature may
vary depending on the presence or absence of material
on the corpse and the environmental conditions where
deceased is located. For example, a smaller body size tends
to cool faster than a larger one due to its higher total surface
area to volume ratio (Lee 2009; Shkrum & Ramsay 2007).
In addition, an obese person can retain body temperature
for a much longer time as compared to a slim person due to
the difference of body fat content (Smart & Kaliszan 2012;
Wardak & Cina 2011). Aside from that, there are some
ante mortem conditions, which may lead to abnormally
high or low body temperature. Condition associated with
heat stroke, fever, stress, hyperthyroidism, brain injury,

malignant hyperthermia, neuroleptic medication, sepsis,


presence of toxins or drugs, ante mortem physical activity
and age of deceased or certain causes of death (such as
suffocation) will lead to abnormal initial body temperature
(Adams 2009b; Smart & Kaliszan 2012).
The common body parts that were used to record
temperature would be intrahepatic, rectum and oral
temperature in some cases (Lee 2009; Swift 2006). Rectal
temperature is normally preferred because it is the easiest
and most accessible way to measure core temperature of
a body without making extra wounds, unless there is issue
of sexual assault or there is no pelvis region left on the
corpse (Hubig et al. 2011; Mall et al. 2005; Muggenthaler
et al. 2012). However, Den Hartog and Lotens (2004)
highlighted some possible sources of error in recording
temperature. These errors include type of thermometer
used, calibration of thermometer, depth of insertion, a
short interval of continuous metabolism rate after death
and special circumstances; for example, fire.
Rigor mortis is the phenomenon of muscle stiffness
on corpse (Parsons 2009; Swift 2006). Autolysis of
sacroplasmic reticulum will release a large amount of
calcium ions and allows binding between actin and myosin
in muscle tissue. Immediately after death, the remaining
ATP in muscle is still sufficient to separate the conjugation
between actin and myosin. However these ATP will soon
deplete, causing the persistent rigidity of muscle to remain
(Powers 2005; Swift 2006).

Rigor mortis involves not only voluntary muscles but
also involuntary muscles with one of the most obvious
signs being cutis anserine or also known as goosebumps
(Powers 2005). It starts from small muscles such as jaw
and eye lids, then downwards to neck, trunk and finally
to bigger muscle mass on upper limbs and lower limbs
(Janaway et al. 2009a; Reddy & Lowenstein 2011). This
is mainly due to the faster ATP loss in smaller muscle mass
compared to larger muscle mass. Rigor mortis will remain
until enzymatic action degrades these binding sites and the
corpse becomes flaccid again. Therefore, inconsistency
of rigor mortis on victim with scenario of crime scene
may give a hint if there is movement of body prior to the
discovery. Surrounding temperature plays an important
factor in the formation of rigor mortis. Higher temperature
environment will lead to faster formation but shorter
duration of rigidity and vice versa for lower temperature
setting (Myburgh 2010; Reddy & Lowenstein 2011).
Rigor mortis is actually different from cadaveric
spasm. Cadaveric spasm or cataleptic rigidity is instant
contraction of muscle at the moment of death and it is
often closely related to the scenario of sudden death or
associated with ante mortem state of mind of intense
emotion (Janaway et al. 2009a; Reddy & Lowenstein
2011). This cadaveric spasm seem to exhibit the scenario
as if the deceased was frozen at his last action in life, which
are related to violent death such as grabbing a weapon or
phone or relating to the circumstances of death.
Livor mortis or hypostasis on the other hand could
be described as the accumulation or pooling of blood at

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the lower part of body due to gravity (Lee 2009; Powers


2005). When blood originated from blood vessels, it
appears visible on the skin as the colour pink, bluish to
dark purplish due to colour of deoxyhemoglobin (Adams
2009b; Myburgh 2010). This development of livor mortis
is different from hemorrhage which is due to blood vessels
puncture and may be differentiated from poisoning which
also show changes in skin colour, such as carbon monoxide,
cyanide, hydrogen sulfide, methemoglobinemia, propane
and in some cases of bacterial infection (Reddy &
Lowenstein 2011; Shkrum & Ramsay 2007).

Before livor mortis is completely fixed, any shifting
of body or pressure may change the pattern of the lividity
otherwise the colour patch will remain permanently visible
on the skin. This criterion is useful in determining any
inconsistency between livor mortis and position of the body
(Dautartas 2009; Reddy & Lowenstein 2011). However,
there might be several pale areas seen at certain body parts.
These are the pressure points where external pressure will
prevent the accumulation of blood at that area. The source
of pressure could originate from body weight load on area
in contact with surface (such as buttocks, midback, calves
and heels) or it may be from a mechanically compressed
area, tight clothing and belt (Adams 2009b; Reddy &
Lowenstein 2011).
STAGES OF DECOMPOSITION

Once the corpse enters putrefaction stage, post mortem


changes and stage of decomposition provide merely a
rough range of PMI due to influence of too many variables
(Myburgh 2010; Shattuck 2009). Stages of decomposition
are mostly determined by post mortem changes observation
or faunal succession pattern analysis (Lee 2009; Myburgh
2010). There are various stages in describing the extent of
decomposition, minor variations often present depending on
point of view of researchers and geographical differences.
There are normally five stages of decomposition process,
which are fresh, bloated, active decay, advanced decay and
skeletal stage but sometimes bloated stage and active decay
are incorporated into one as early decay stage. Observations
used to describe the decomposition process are generally
applicable everywhere because all corpses decompose
with similar pattern of decomposition. However, the rate
of decomposition may appear different even within the
same district simply due to microclimate, topographical
and geographical differences. Local studies found that
decomposition process in Malaysia actually progress
at a much faster rate compared with other countries in
temperate climate (Heo et al. 2007; Teo et al. 2013).
Fresh stage starts immediately at the moment of
death. Autolysis cellular destruction occurs in this stage
and leads to early post mortem changes, including the
aforementioned algor mortis, rigor mortis and livor mortis
(Lee 2009; Voss et al. 2008). There is no strong odour of
decomposition in fresh stage until the corpse has reached
bloated stage (Mcquinn 2011; Shattuck 2009). However
soon after death, arthropod activity will start mostly with

1876

arrival of flies. Previous studies showed that Dipteran is the


earliest arthropod that arrives at the corpse (Campobasso et
al. 2001; Vitta et al. 2007). Dipteran usually choose natural
orifices (eyes, nose, mouth, genital), hair and crevices of
corpse as site for oviposition (Ahmad & Ahmad 2009;
Cross & Simmons 2010).
Bloating is the distension or swelling of body
parts due to accumulation of decompositional products
(mainly gas) produced by microorganism in anaerobic
putrefaction at any anatomically possible spaces in body,
included organs and soft tissues. (Dekeirsschieter et al.
2009; Gebhart et al. 2012). Bloating normally starts at
abdomen then slowly expands to other body parts, which
include genital and face with eye and tongue protrusion
(Dekeirsschieter et al. 2009; Gennard 2007). According to
Genhart et al. (2012), bloating of corpse is normally noted
to be in symmetrical pattern and any violation may indicate
hidden injury or temperature variation. The accumulation
of decompositional products will continue up to an extent
where the corpse will collapse followed by release of the
gas, fluid and salt into the surrounding from all possible
orifices of corpse (Carter et al. 2007; Enwere 2008).
At the same time, hydrolytic enzymes digest the
junction between dermis, causing blister to appear on the
skin and in some cases the stratum corneum to detach
(Lee 2009; Shkrum & Ramsay 2007). Skin slippage at
hand and feet is common and often known as degloving
phenomenon (Powers 2005; Shkrum & Ramsay 2007).
Bloating is often noticed together with marbling when
arteries and veins are visible on skin appearance due to
formation of sulf-hemoglobin from bacterial reaction in
blood vessels (Powers 2005; Shkrum & Ramsay 2007).
The changes may gradually shift into larger discoloration
of skin with range of discoloration varying from green,
brown and grey to black in colour (Parsons 2009; Shattuck
2009).

When post bloating of the corpse occurs, decomposition
process proceeds into active decay stage. The rate of
degradation turns faster because rupture of skin integration
opens extra access points for microorganisms, arthropods
and scavengers. The ruptured skin of corpse may turn
black accompanied by hair loss (Shkrum & Ramsay 2007).
Liquefaction of soft tissues starts with the presence of froth
while extremities of corpse may desiccate in some cases
(Parsons 2009; Sharanowski et al. 2008). At this level,
the activity of Dipteran larvae is at maximum with fast
consumption of soft tissue and some species of Coleoptera
may be present (Carter et al. 2007; Matuszewski et al.
2008).
The decomposition process is then followed by
advanced decay stage, which is also known as black
putrefaction or late decaying stage. Bone exposure starts
and the overall corpse shows caving in appearance with
some higher degradation-resistant tissues left behind such
as cartilage, hair and desiccated tissue (Dekeirsschieter
et al. 2009; Sharanowski et al. 2008). There is only weak
odour of decaying smell or cheesy odour in this stage

(Ahmad & Ahmad 2009; Sharanowski et al. 2008). One


of the major indicators for this stage is major migration
of Dipteran larvae for pupation (Matuszewski et al. 2008;
Sharanowski et al. 2008). Population of Dipteran species
is gradually replaced by Coleoptera species as part of the
faunal succession pattern (Ahmad et al. 2011; Voss et al.
2008, 2011).
Dry remains or skeletal stage is reached when
there is a very high degree of bone exposure but
extreme breakdown of the bone material has not started
(Sharanowski et al. 2008; Swann et al. 2010b). Adlam
and Simmons (2007) defined skeletonization in their
studies as any one of: only spine was left underneath
dried skin accompanied by major loss of intra-abdominal
tissue; higher than 50% of bone exposure with minimal
moisture; or more than 30% of bones already underwent
bleaching and weathering process (Adlam & Simmons
2007). During this stage, only a very few amount of
dried skin, tendon and cartilage will present. Minimal
moisture from environment or grease may present on the
bone surface and the smell of decomposition generally
fades off (Matuszewski et al. 2008). Some insect species
are still present in this stage but mostly from Coleoptera
and Acari (mites) (Ahmad et al. 2011; Braig & Perotti
2009). Sequence of skeletonization may vary depending
on environmental setting and condition of the corpse. It
is believed that under normal circumstances, head, face
and limbs will decompose faster than the corpse but this
sequence is subject to any variation caused by position of
corpse and environmental setting (Bachmann & Simmons
2010; Dautartas 2009).
When the corpse reached the skeletal stage,
decomposition slows down dramatically and progress at
timeframe of years or decades. The bones will undergo
process of microbial attack of collagen; weathering,
bleaching, exfoliation, cracking of cortical bone (followed
by exposure of trebacular bone), loss of its inorganic
mineral content and invasion of vegetation root (Shattuck
2009; Vass 2001). PMI at this stage may be difficult to
determine although there are methods to examine skeletal
remains based on completeness, fragmentation and
articulation or weathering effect (Lieverse et al. 2006;
Ross & Cunningham 2011). Ross and Cunningham (2011)
estimated that complete decomposition of bones require
time between six to thirty years in a tropical environment
setting.
In real forensic context, different body parts of a
corpse decompose at different speed thus different stages
of decomposition could be observed on the same corpse
simultaneously. It could be challenging for forensic
pathologists to use a single stage of decomposition to
describe the extent of degradation of a corpse (Adlam &
Simmons 2007; Duday & Guillon 2006). It is generally
accepted that head and limbs will decompose faster
compared to body trunk, mainly because there is a higher
concentration of soft tissue to be digested (Braig & Perotti
2009; Matuszewski et al. 2008).

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MUMMIFICATION

Mummification is a process of desiccation that occurs at


tissue of corpse, mostly induced by dry environment or
air current, high temperature or situation that is low in
humidity (Gennard 2007; Schotsmans et al. 2011b). It
originates from the Persian word mmiya which means
bitumen (Schotsmans et al. 2011b). In mummification, the
most significant observation is the skin will turn into dark
brown with hard, leathery and parchment-like appearance
(Janaway et al. 2009b; Schotsmans et al. 2011b).
Dehydration of body tissues allows the preservation of the
corpse for a longer period (Carter et al. 2007; Janaway et al.
2009b). This is mainly because the moisture content is not
adequate for microorganism activity of tissue degradation,
causing decomposition to be hindered (Janaway et al.
2009b; Powers 2005). The corpse loses its moisture
content and tissue mass volume, leaving behind skin that
then further shrinks into smaller volume. In some cases,
the extreme shrinkage at joints will tear the skin apart
especially at groin, neck and armpit area.

A thin corpse is more susceptible to mummification
as compared to an obese due to difference in muscle bulk
and adipose tissue (Reddy & Lowenstein 2011; Schotsmans
et al. 2011b). Newborn babies also tend to mummify as
they are relatively sterile in their gastrointestinal tracts
and thus there is no microorganism population to kick
start the putrefaction internally (Janaway et al. 2009b;
Schotsmans et al. 2011b). Also, the presence of good air
flow and any covering or clothing made of material that
facilitate evaporation of fluids from body may indirectly
enhance formation of a mummified corpse (Janaway et al.
2009a; Teo et al. 2013).

Mummification of a corpse could occur as whole
body mummification or at localized body parts such as
fingers, tongue and toes (Forbes et al. 2005; Janaway et al.
2009b). Mummification may occur on internal organs as
well although they are often to be the last part observed to
mummify (Mcquinn 2011; Schotsmans et al. 2011b). When
the skin of a corpse mummify, the preservation of internal
organs depends on the extent of putrefaction and autolysis
when the environmental setting favours mummification
(Janaway et al. 2009a). Therefore, the internal organs
may appear moist while the skin is already mummified
(Janaway et al. 2009b; Parsons 2009). Generally, it is
also accepted that burial with soil of coarse properties
(such as sand) allow dehydration of tissues thus enhancing
mummification (Carter et al. 2007; Gaudry 2010).
Schotsmans et al. (2011a) also concluded that burial with
the presence of quicklime will induce mummification of
corpse at skin level, but not including the internal organs.
ADIPOCERE

Adipocere is a consistent, greasy, wax-like appearance of


substance with the colour ranging from yellowish white
to gray in colour (Notter et al. 2009; Ubelaker & Zarenko
2011). It can preserve soft tissue, internal organs or the
whole corpse by inhibiting bacterial reaction, arthropod

and animal scavenging activity (Fiedler et al. 2004; Forbes


et al. 2005). For example, preservation of hyoid bone
fracture and toxicology evidence preserved in internal
organs can help in determining accurate cause of death
for deceased (Ubelaker & Zarenko 2011). Adipocere
actually originates from Latin words, adipo or adeps
meaning fat and cera or cere meaning wax (Ubelaker
& Zarenko 2011; Widya et al. 2012). The formation of
adipocere also known as saponification, is another form
of variation of post mortem changes that can preserve
the corpse for a significant period of time (Dures et al.
2010; Fiedler et al. 2004). However, the formation of
adipocere will adversely affect identification of deceased
and PMI estimation (Pinheiro & Cunha 2006; Widya et al.
2012). The species of bacteria involve in the formation of
adipocere include Clostridium perfringens and Clostridium
frigidicanes (Vass 2001; Widya et al. 2012). Previous
studies showed that formation of adipocere require moist
and anaerobic condition (Ubelaker & Zarenko 2011; Widya
et al. 2012). However, several previous studies documented
that adipocere can also be found on corpses discovered
from sea bed (Anderson 2010; Ubelaker & Zarenko 2011).

Previous studies proved that formation of adipocere
normally starts from adipose tissue in the body (Forbes et
al. 2005; Wilson et al. 2007). Obese individual, female, the
elderly and babies have higher tendency to form adipocere
as compared to thin individual, male and adult due to the
variation of fat property and composition (Fiedler & Graw
2003; Schotsmans et al. 2011b). Hydrolysis of triglyceride
by bacterial action yields a mixture of free fatty acids and
the unsaturated fatty acids will transform into saturated
fatty acids via oxidation, hydration or hydrogenation
(Fiedler et al. 2004; Notter et al. 2009). The types saturated
fatty acid mainly consist of palmitic, stearic and myristic
acid (Dures et al. 2010; Notter et al. 2009). The fatty acids
will then interact with inorganic ions and form salts.

There are some controversy among scientists about the
difference between soft paste-like adipocere and hardened
brittle armour-like adipocere. Powers (2005) mentioned
that the soft paste adipocere is made of conjugation with
sodium ion and the latter one mainly with potassium ion.
However, Fiedler et al. (2004) and Vass (2001) stated the
opposite way with addition of magnesium ion and calcium
ion in producing brittle adipocere other than sodium ion.
Some researchers believe that the soft paste adipocere will
eventually harden with time (Notter et al. 2009; Wilson et
al. 2007). This makes sense since there might be exchange
of ions in salts meanwhile evaporation of fluids along
times.
It is generally believed that formation of adipocere
is related to burial with soil of fine texture property, loam
enriched, low in permeability and poor drainage property
(Dures et al. 2010). High clay, silt and lime content that
increase alkaline value of soil will further enhance the
formation of adipocere (Fiedler & Graw 2003; Schotsmans
et al. 2011a). This is because these soil properties entrap
the fluid released during decomposition around the corpse,
which is essential for transformation of adipose tissue into

1878

adipocere. Some studies proved that moisture content


inside body itself is already sufficient for formation of
adipocere (Carter et al. 2007). It is also believed that the
formation of adipocere is normally associated with clothing
and/or covering (Fiedler et al. 2012; Forbes et al. 2005).
However, the variety of fabric used and their properties
are too wide, causing their roles in enhancing or inhibiting
formation of adipocere to remain unclear. Researches by
Dautartas (2009) and Shirley et al. (2011) mentioned that
the presence of plastic wrapping will enhance formation of
adipocere. Meanwhile, Forbes et al. (2005) found that the
impermeable property of plastic may cause accumulation
of waste product and inhibition of free saturated fatty acids
from interacting with soil to transform into adipocere.
Although the adipocere formed will retard the
decomposition process, adipocere itself is also subject
to decomposition once it is exposed to aerobic condition
(Fiedler et al. 2012; Wilson et al. 2007). Population
involved in decomposition of adipocere is mainly Grampositive bacteria such as Bacillius sp., Cellulomonas sp.
and Nocardia sp. (Fiedler & Graw 2003; Fiedler et al.
2004).
BURIED CORPSE

Undoubtedly, a corpse will always be the most important


evidence in homicide case and criminals often choose to
conceal the corpse from law enforcement. Burial is one of
the methods that can be used to hide the corpse from public
attention (Enwere 2008; Prangnell & Mcgowan 2009). This
type of shallow clandestine grave often ranges from 0.3
to 0.7 m depth compared to legal graveyard with graves
at 1.2 to 1.4 m depth (Hoffman et al. 2009; Prangnell &
Mcgowan 2009). The site chosen for clandestine graves
commonly follows these criteria such as geographically
located at an area of short distance away from rarely used
pathways or roads, roughly ten feet next to the nearest
large tree, surrounded by bushes, shrubs or leafage with
the corpse clothed (or wrapped) (Hoffman et al. 2009).

It is generally accepted that corpses buried underground
decompose slower compared to corpses left on ground
surface (Campobasso et al. 2001; Teo et al. 2013).
According to Caspers rule, a buried corpse requires eight
times longer than a corpse decaying on ground surface to
reach the same stage of decomposition (Fiedler & Graw
2003; Gennard 2007). Depth of grave plays an essential
role in determining to what extent the slowing down of
decomposition will be. Research done by Rodriguez is
one of the earliest of its kind in taphonomy field and he
found that corpses buried at 0.3 to 0.6 m depth takes several
months up to a year to reach dry remains stage while 0.9
to 1.2 m depth require years before the corpse is fully
skeletonized (Gaudry 2010; Shattuck 2009).

The main reason for the slower rate of decomposition
is due to the restricted access for majority of insect and
scavenger animals at buried corpse (Campobasso et al.
2001; Ross & Cunningham 2011). However, buried corpse
actually has its own faunal succession pattern, which is

different from that on a ground surface corpse. Some


species of Dipteran are able to move through the soil layer
to reach the corpse or they lay eggs on the ground surface
and the hatched larvae then moves down onto the corpse
through rain infusion; such as Muscidae, Phoridae and
Callophoridae (in some cases) (Gaudry 2010; Myburgh
2010). Common entomological evidences that could be
collected from buried corpse can be categorized into
Arachnida (such as Acari, Diplopoda and Araneae) and also
Insecta (which include Diptera, Coleoptera, Dermaptera,
Collembola, Thysanura, Blattodea and Hymeonoptera)
(Gaudry 2010; Gennard 2007).
Preburial exposure of corpse towards arthropod
activity may enhance decomposition process compared
with those without exposure by attracting the early waves
of decomposer arthropods. However, even if there is
preburial exposure to arthropod activity, there is lack of
subsequent wave of insect from normal faunal succession
and there will not be a real larvae mass on buried corpses
(Bachmann & Simmons 2010; Dautartas 2009). Therefore,
decomposition in graves mainly relies on microbiological
activity, with population from both gastrointestinal tract
and surrounding soil (Carter & Tibbett 2008; Wilson et al.
2007).

Lower temperature in grave as compared to ambient
temperature is another reason for slower decomposition of
a buried corpse. The soil layer above the grave functions as
an insulator and block the heat energy from solar radiation
(Myburgh 2010; Prangnell & Mcgowan 2009). Combined
with the soil thermal heat storage capacity on its own, the
temperature in grave fluctuates in a smaller magnitude
compared to ground surface (Prangnell & Mcgowan 2009).
However, the temperature inside the grave is still adequate
for microbial metabolism. With the increase of depth,
temperature will be lower and thus slower the degradation
of tissue (Bachmann & Simmons 2010; Schultz 2008).
The low oxygen content underground also restricts the
microbial population to only anaerobic strands thus also
delaying the decomposition process (Dent et al. 2004;
Statheropoulos et al. 2011).

A corpse decays faster when in contact with soil and
hence every material that separate corpse from soil will
delay rate of decomposition (Duday & Guillon 2006).
Examples of these include clothing, grave and bedding
material. Coffin made of pine and spruce will enhance
degradation of corpse while oak, lead and zinc coffin will
retard the decomposition process (Fiedler & Graw 2003).
Mller et al. (2011) also found that coffin that contain high
amount of heavy metal can preserve the buried corpse by
inhibiting microbial metabolism. However, commercial
coffin nowadays actually enhance decomposition because
its absorbent property facilitates dissolution of soft tissue
and prevent formation of adipocere (Dautartas 2009;
Gaudry 2010). Meanwhile, air void in coffin allows a small
extent of aerobic condition that supports aerobic microbial
population or survival of some arthropods if there was
preburial exposure (Dautartas 2009; Janaway et al. 2009b).

Air tight coffin on the other hand will inhibit the dispersion
of decompositional products which then turn into toxic thus
delaying decomposition (Ross & Cunningham 2011).
When the corpse buried in grave has reached dry
remains stage, the position of bone may change due to
decay of tissue and force of gravity if there is free space
around the corpse (Duday & Guillon 2006). The PMI may be
even harder to be determined when the corpse has reached
skeletonization stage. Study done by Jaggers and Rogers
(2009) found that there is no change in colour, texture or
even overall condition of pig bones after five months of
post burial period.

In buried cases, the presence of wounds or penetrative
trauma seem to be not as significant as compared with
corpses that decompose on ground surface because there
is less chances of arthropod oviposition on the wounds
(Bachmann & Simmons 2010; Cross & Simmons 2010).
At the same time, repeated burial in the same grave will
accelerate the rate of decomposition due to the ready
presence of rich microbiology population which is
optimum in decaying organic matter (Carter & Tibbett
2008; Pringle et al. 2010). However, study done by
Fiedler and Graw (2003) found that humus produced by
previously buried corpse may cause the surrounding soil
spores in grave to become smaller and cause higher fluid
retention for the subsequent buried corpse hence delaying
the decomposition process. This phenomenon is the same
for corpses buried directly in soil with high amount of clay,
which has a higher fluid retention property. The experiment
done by Schultz (2008) and Schultz et al. (2006) used
buried pig carcass at soil with high composition of clay
showed signs of soft tissue preservation after one year
regardless of the size of pig used.
Several previous studies linked released chemical
compound or odour analysis to PMI estimation (Paczkowski
& Schtz 2011; Swann et al. 2010a). Review done by
Swann et al. (2010b) explained analytical instruments
used in analyzing various decompositional products and
the benefits in understanding the process of decomposition.
Vass et al. (2004) studied the volatile decompositional
products that could be detected on ground surface for
various depths of burial. There are eight major classes
of products, which include cyclic and non-cyclic
hydrocarbon, nitrogen compound, sulfur compound,
oxygen compound, halogen compound, acid and ester
compound. Another similar research further identified
the key volatile compounds which are related to either
soft tissue degradation or breakdown of bone component
(Vass et al. 2008). Nitrogen-reactive ninhydrin and fatty
acids in gravesoil as product from degradation of fat and
protein could also be analyzed to provide a certain range
of PMI or in locating a grave (Swann et al. 2010a; Tibbett
& Carter 2009).

Research done by Vass et al. (2004) showed the first
volatile compound was detected on ground surface at 17
days for a 1.5 feet depth grave, while a 2.5 feet grave needs
two months and above for the first volatile decompositional
product to be detected. Factors that affecting release of

1879

decompositional product include temperature, moisture,


soil pH value and the availability of oxygen in burial (Vass
et al. 2008). Dalva et al. (2012) also stated that for deep
burial, the chemical product released from decomposition
might be utilized by neighboring microbiology population
as substrate and hence not detected. In other words, the
compound detected on ground surface for deep graves
may not have originate from the decaying corpse but is a
product from metabolism of other soil population that is
not related to degradation process as predicted by Vass et
al. (2004).
CONCLUSION
Decomposition is a sophisticated process representing
how a corpse slowly degrades into brick components and
is gradually recycled into the environment by decomposer
activities, such as microorganisms, invertebrates and
vertebrate fauna. The degradation process from a fresh
cadaver to dry skeletal remains until the destruction of
bone element takes time from years if not centuries, if
variations such as mummification and adipocere occur.
However, the decomposition process itself is subject
to various intrinsic such as age, weight, ante mortem
condition, presence of trauma, drugs or toxin and extrinsic
factors such as environment setting, temperature,
moisture level, sun exposure, layers and type of clothing,
coffin and bedding and accessibility of insect. In fact, the
condition of corpses in real crime scene is often diverse
and numerous variables may have taken part in leading
to the point of decomposition process before the arrival
of experts. Therefore, it is difficult to compare between
studies and real cases due to differences in climate,
geographical location, subject or model used and setting
of the study. Analysis for case reports should not rely
solely on single taphonomic research, which mostly
focuses on a few variables at one time. Nevertheless,
estimation of PMI plays a very important role not only
in the investigation of suspect and manner of death,
but also assists the jurisdictional system in making the
right decision. At the end of the day, there is no single
estimation method that can provide a precise moment
of PMI above all but in range of hours until years, thus
combination between different approaches of estimation
is necessary to increase the accuracy of PMI. Although
there are extensive forensic taphonomic studies conducted
to study how different variables affecting decomposition
process, the correlation between different factors is yet
to be uncovered in detail.
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School of Diagnostic & Applied Health Sciences
Faculty of Health Sciences
Universiti Kebangsaan Malaysia
43600 Bangi, Selangor
Malaysia
*Corresponding author; email: drsripaah@gmail.com
Received: 19 January 2014
Accepted: 25 April 2014